Trophic complexity and the adaptive value of damage-induced plant volatiles

Abstract

Indirect plant defenses are those facilitating the action of carnivores in ridding plants of their herbivorous consumers, as opposed to directly poisoning or repelling them. Of the numerous and diverse indirect defensive strategies employed by plants, inducible volatile production has garnered the most fascination among plant-insect ecologists. These volatile chemicals are emitted in response to feeding by herbivorous arthropods and serve to guide predators and parasitic wasps to their prey. Implicit in virtually all discussions of plant volatile-carnivore interactions is the premise that plants "call for help" to bodyguards that serve to boost plant fitness by limiting herbivore damage. This, by necessity, assumes a three-trophic level food chain where carnivores benefit plants, a theoretical framework that is conceptually tractable and convenient, but poorly depicts the complexity of food-web dynamics occurring in real communities. Recent work suggests that hyperparasitoids, top consumers acting from the fourth trophic level, exploit the same plant volatile cues used by third trophic level carnivores. Further, hyperparasitoids shift their foraging preferences, specifically cueing in to the odor profile of a plant being damaged by a parasitized herbivore that contains their host compared with damage from an unparasitized herbivore. If this outcome is broadly representative of plant-insect food webs at large, it suggests that damage-induced volatiles may not always be beneficial to plants with major implications for the evolution of anti-herbivore defense and manipulating plant traits to improve biological control in agricultural crops.

Figure 1. A simple three-trophic level conceptual model based on the well-studied mechanistic linkages between cotton (Gossypium hirsutum), the herbivorous insect Helicoverpa zea, and the parasitic wasp Microplitis croceipes.

Solid blue arrows denote who eats whom, whereas dashed black arrows highlight ecological effects spanning non-adjacent trophic levels. Chemical structures represent caterpillar-induced cotton volatiles known to impact parasitoid foraging behavior, e.g., ,; from top to bottom: linalool, 3,7-dimethyl-1,3,6-octatriene, caryophyllene, and cis-3-hexen-1-ol. Photo credits: cotton, Charles T. Bryson, USDA-ARS, Bugwood.org; H. zea, Peggy Greb, USDA-ARS, Bugwood.org; Microplitis sp., James Lindsey, Ecology of Commanster.

Figure 2. A food web depiction of feeding relationships associated with the caterpillar

The trophic diagram is based on direct field observations of predation events by W.H. Whitcomb and K. Bell in Arkansas (US) cotton fields during the 1950s and 1960s, and later reconstructed by . Only a small subset of the carnivore community was included for ease of presentation and the food web thus represents a highly simplified view of trophic dynamics that naturally occur in this system. Photo credits: cotton, Charles T. Bryson, USDA-ARS; H. zea, Peggy Greb, USDA-ARS; jumping and lynx spiders and damsel bug, Joseph Berger; crab spider, Frank Peairs, Colorado State University; lady beetle, Scott Bauer, USDA-ARS; big-eyed bug and paper wasp, Russ Ottens, University of Georgia; assassin bug, Clemson University, USDA Cooperative Extension; praying mantis and robber fly, Whitney Cranshaw, Colorado State University; minute pirate bug, Bradley Higbee, Paramount Farming; mud dauber, used with permission from entomart (image available via www.entomart.be). All images (except for the mud dauber) are from Bugwood.org.